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Enhanced survival of ischemic skin flap by combined treatment with bone marrow-derived stem cells and low-level light irradiation

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Abstract

The aim of this study is to examine the enhanced survival effect of ischemic skin flap by combined treatment with bone marrow-derived stem cells (BMSCs) and low-level light irradiation (LLLI). The neovasculogenic effect of BMSCs induced by LLLI was detected using a wound healing and tube formation assay. ICR mice were divided into four groups: control group, LLLI group, BMSCs group, and combine-treated group. The percentage of skin flap necrosis area was calculated on the seventh post-operative day. Specimens were harvested for histologic analyses. LLLI promoted BMSC migration and tube formation. The flap survival rate of combined treated group was significantly higher than that of the control group. Histologic results demonstrated a significant increase in neovascularization in the combined treatment group. This study demonstrates that combination treatment of BMSCs and LLLI could enhance the survival of ischemic skin flap in a mouse model.

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References

  1. Risau W (1997) Mechanisms of angiogenesis. Nature 386:671–674

    Article  CAS  PubMed  Google Scholar 

  2. Tepper OM, Galiano RD, Kalka C, Gurtner GC (2003) Endothelial progenitor cells: the promise of vascular stem cells for plastic surgery. Plast Reconstr Surg 111:846–854

    Article  PubMed  Google Scholar 

  3. Lyden D, Hattori K, Dias S et al (2001) Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 7:1194–1201

    Article  CAS  PubMed  Google Scholar 

  4. Simman R, Craft C, McKinney B (2005) Improved survival of ischemic random skin flaps through the use of bone marrow nonhematopoietic stem cells and angiogenic growth factors. Ann Plast Surg 54:546–552

    Article  CAS  PubMed  Google Scholar 

  5. Ichioka S, Kudo S, Shibata M, Ando J, Sekiya N, Nakatsuka T (2004) Bone marrow cell implantation improves flap viability after ischemia-reperfusion injury. Ann Plast Surg 52:414–418

    Article  PubMed  Google Scholar 

  6. Corazza AV, Jorge J, Kurachi C, Bagnato VS (2007) Photobiomodulation on the angiogenesis of skin wounds in rats using different light sources. Photomed Laser Surg 25:102–106

    Article  PubMed  Google Scholar 

  7. Kipshidze N, Nikolaychik V, Keelan MH et al (2001) Low-power helium: neon laser irradiation enhances production of vascular endothelial growth factor and promotes growth of endothelial cells in vitro. Lasers Surg Med 28:355–364

    Article  CAS  PubMed  Google Scholar 

  8. Hou JF, Zhang H, Yuan X, Li J, Wei YJ, Hu SS (2008) In vitro effects of low-level laser irradiation for bone marrow mesenchymal stem cells: proliferation, growth factors secretion and myogenic differentiation. Lasers Surg Med 40:726–733

    Article  PubMed  Google Scholar 

  9. Abramovitch-Gottlib L, Gross T, Naveh D et al (2005) Low level laser irradiation stimulates osteogenic phenotype of mesenchymal stem cells seeded on a three-dimensional biomatrix. Lasers Med Sci 20:138–146

    Article  PubMed  Google Scholar 

  10. Arnaoutova I, Kleinman HK (2010) In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nat Protoc 5:628–635

    Article  CAS  PubMed  Google Scholar 

  11. Tang YH, Pennington LA, Scordino JW, Alexander JS, Lian T (2016) Dynamics of early stem cell recruitment in skin flaps subjected to ischemia reperfusion injury. Pathophysiology 23(3):221–228

    Article  PubMed  Google Scholar 

  12. Schweizer R, Kamat P, Schweizer D et al (2014) Bone marrow-derived mesenchymal stromal cells improve vascular regeneration and reduce leukocyte-endothelium activation in critical ischemic murine skin in a dose-dependent manner. Cytotherapy 16(10):1345–1360

    Article  CAS  PubMed  Google Scholar 

  13. Lamalice L, Le Boeuf F, Huot J (2007) Endothelial cell migration during angiogenesis. Circ Res 100:782–794

    Article  CAS  PubMed  Google Scholar 

  14. Maleki M, Ghanbarvand F, Reza Behvarz M, Ejtemaei M, Ghadirkhomi E (2014) Comparison of mesenchymal stem cell markers in multiple human adult stem cells. Int J Stem Cells 7:118–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Liu L, Gao J, Yuan Y, Chang Q, Liao Y, Lu F (2013) Hypoxia preconditioned human adipose derived mesenchymal stem cells enhance angiogenic potential via secretion of increased VEGF and bFGF. Cell Biol Int 37:551–560

    Article  CAS  PubMed  Google Scholar 

  16. Sun XT, Ding YT, Yan XG et al (2004) Angiogenic synergistic effect of basic fibroblast growth factor and vascular endothelial growth factor in an in vitro quantitative microcarrier-based three-dimensional fibrin angiogenesis system. World J Gastroenterol: WJG 10:2524–2528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Yang M, Sheng L, Li H, Weng R, Li QF (2010) Improvement of the skin flap survival with the bone marrow-derived mononuclear cells transplantation in a rat model. Microsurgery 30:275–281

    Article  PubMed  Google Scholar 

  18. Cury V, Moretti AI, Assis L et al (2013) Low level laser therapy increases angiogenesis in a model of ischemic skin flap in rats mediated by VEGF, HIF-1alpha and MMP-2. J Photochem Photobiol B 125:164–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Uysal AC, Mizuno H, Tobita M, Ogawa R, Hyakusoku H (2009) The effect of adipose-derived stem cells on ischemia-reperfusion injury: immunohistochemical and ultrastructural evaluation. Plast Reconstr Surg 124:804–815

    Article  CAS  PubMed  Google Scholar 

  20. Prado RP, Liebano RE, Hochman B, Pinfildi CE, Ferreira LM (2006) Experimental model for low level laser therapy on ischemic random skin flap in rats. Acta cirurgica brasileira/Sociedade Brasileira para Desenvolvimento Pesquisa em Cirurgia 21:258–262

    Article  Google Scholar 

  21. Briers JD, Fercher AF (1982) Retinal blood-flow visualization by means of laser speckle photography. Invest Ophthalmol Vis Sci 22:255–259

    CAS  PubMed  Google Scholar 

  22. Boas DA, Dunn AK (2010) Laser speckle contrast imaging in biomedical optics. J Biomed Opt 15:011109

    Article  PubMed  PubMed Central  Google Scholar 

  23. Lu F, Mizuno H, Uysal CA, Cai X, Ogawa R, Hyakusoku H (2008) Improved viability of random pattern skin flaps through the use of adipose-derived stem cells. Plast Reconstr Surg 121:50–58

    Article  CAS  PubMed  Google Scholar 

  24. Horvat-Karajz K, Balogh Z, Kovacs V, Drrernat AH, Sreter L, Uher F (2009) In vitro effect of carboplatin, cytarabine, paclitaxel, vincristine, and low-power laser irradiation on murine mesenchymal stem cells. Lasers Surg Med 41:463–469

    Article  PubMed  Google Scholar 

  25. Keck PJ, Hauser SD, Krivi G et al (1989) Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 246:1309–1312

    Article  CAS  PubMed  Google Scholar 

  26. Folkman J, Klagsbrun M (1987) Angiogenic factors. Science 235:442–447

    Article  CAS  PubMed  Google Scholar 

  27. Suri C, Jones PF, Patan S et al (1996) Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87:1171–1180

    Article  CAS  PubMed  Google Scholar 

  28. Yang EY, Moses HL (1990) Transforming growth factor beta 1-induced changes in cell migration, proliferation, and angiogenesis in the chicken chorioallantoic membrane. J Cell Biol 111:731–741

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health and Welfare, Republic of Korea (grant number: HI14C1234).

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Correspondence to Phil-Sang Chung.

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The authors declare that they have no conflicts of interest.

Ethical approval and informed consent

This animal study was performed according to the IRB, which was approved by the Ethics Committee of Dankook University (DKU-13-043).

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Moon, J.H., Rhee, YH., Ahn, JC. et al. Enhanced survival of ischemic skin flap by combined treatment with bone marrow-derived stem cells and low-level light irradiation. Lasers Med Sci 33, 1–9 (2018). https://doi.org/10.1007/s10103-017-2312-9

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  • DOI: https://doi.org/10.1007/s10103-017-2312-9

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